Skip to main content
SpringerLink
Log in

Overexpression of miR319a Altered Oil Body Morphogenesis and Lipid Content in Arabidopsis Seeds

  • Original paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

MicroRNA319a (miR319a) acts as an essential regulator of gene expression during plant development and under stress conditions. Although the role of miR319a in regulating leaf development has been well studied in Arabidopsis, the function of miR319a in regulating seed oil content remains poorly understood. To examine the effects of miR319a on oilseed oil bodies (OBs) and oil content, miR319a was overexpressed in Arabidopsis in this study. Overexpression of 35S:miR319a in transgenic Arabidopsis caused severely crinkled siliques and led to increased total oleosin levels. Electron microscopy revealed that the overexpression of miR319a in transgenic Arabidopsis seeds resulted in more numerous and smaller OBs compared to WT plants, suggesting an inverse relationship between OB size and oleosin levels. Changes in the size of OBs altered the accumulation of lipids and decreased seed lipid contents to 10% in 35S:miR319a-12 and to 6% in 35S:miR319a-85, which were lower than the WT control. The fatty acid profiles indicated that palmitic, linoleic, linolenic, and eicosenoic acids increased by 15.2%, 5.2%, 17.6%, and 26.9%, respectively, on average, compared to WT seeds. Increases in these four fatty acids were compensated by a 24.7% and 38.4% decrease in oleic and erucic acids, respectively. Therefore, these results imply that miR319a is involved in lipid metabolism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Prog Lipid Res 49:235–249

    Article  CAS  Google Scholar 

  • Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C (2018) Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol 176:1694–1708

    Article  CAS  Google Scholar 

  • Chen JC, Tsai CC, Tzen JT (1999) Cloning and secondary structure analysis of caleosin, a unique calcium-binding protein in oil bodies of plant seeds. Plant Cell Physiol 40:1079–1086

    Article  CAS  Google Scholar 

  • Chen K, Yin YT, Liu S, Guo ZY, Zhang K, Liang Y, Zhang LN, Zhao WG, Chao HB, Li MT (2019) Genome-wide identification and functional analysis of oleosin genes in Brassica napus L. BMC Plant Biol 19:294

    Article  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  Google Scholar 

  • Gu JW, Chao HB, Wang H, Li YH, Li DR, Xiang J, Gan JP, Lu GY, Zhang XK, Long Y, Li MT (2016) Identification of the relationship between oil body morphology and oil content by microstructure comparison combining with QTL analysis in Brassica napus. Front Plant Sci 7:1989

    PubMed  Google Scholar 

  • Hu ZY, Wang XF, Zhan GM, Liu GH, Hua W, Wang HZ (2009) Unusually large oilbodies are highly correlated with lower oil content in Brassica napus. Plant Cell Rep 28:541–549

    Article  CAS  Google Scholar 

  • Huang AH (1996) Oleosins and oil bodies in seeds and other organs. Plant Physiol 110:1055–1061

    Article  CAS  Google Scholar 

  • Kim HU, Hsieh K, Ratnayake C, Huang AHC (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J Biol Chem 277:22677–22684

    Article  CAS  Google Scholar 

  • Krahmer N, Guo Y, Wilfling F, Hilger M, Lingrell S, Heger K, Newman HW, Schmidt-Supprian M, Vance DE, Mann M, Farese RV, Walther TC (2011) Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP: phosphocholine cytidylyltransferase. Cell Metab 14:504–515

  • Liu RH, Lehane S, He XL, Lehene M, Hertz-Fowler C, Berriman M, Pickett JA, Field LM, Zhou JJ (2010) Characterisations of odorant-binding proteins in the tsetse fly Glossina morsitans morsitans. Cell Mol Life Sci 67:919–929

  • Liu WX, Liu HL, Qu LQ (2013) Embryo-specific expression of soybean oleosin altered oil body morghogenesis and increased lipid content in transgenic rice seeds. Theor Appl Genet 126:2289–2297

    Article  CAS  Google Scholar 

  • Lu CF, Fulda M, Wallis JG, Browse J (2006) A high-throughput screen for genes from castor that boost hydroxy fatty acid accumulation in seed oils of transgenic Arabidopsis. The Plant J 45:847–856

    Article  CAS  Google Scholar 

  • Mansfield SG, Briarty LG (1992) Cotyledon cell development in Arabidopsis thaliana during reserve deposition. Can J Bot 70:151–164

  • Miquel M, Trigui G, d'Andrea S, Kelemen Z, Baud S, Berger A, Deruyffelaere C, Trubuil A, Lepiniec L, Dubreucq B (2014) Specialization of oleosins in oil body dynamics during seed development in Arabidopsis seeds. Plant Physiol 164:1866–1878

    Article  CAS  Google Scholar 

  • Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci U S A 106:22534–22539

    Article  CAS  Google Scholar 

  • Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407

    Article  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu XL, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  CAS  Google Scholar 

  • Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:1991–2001

    Article  CAS  Google Scholar 

  • Shimada TL, Hara-Nishimura I (2010) Oil-body-membrane proteins and their physiological functions in plants. Biol Pharm Bull 33:360–363

    Article  CAS  Google Scholar 

  • Shimada TL, Shimada T, Takahashi H, Fukao Y, Hara-Nishimura I (2008) A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. The Plant J 55:798–809

    Article  CAS  Google Scholar 

  • Siloto RM, Findlay K, Lopez-Villalobos A, Yeung EC, Nykiforuk CL, Moloney MM (2006) The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis. Plant Cell 18:1961–1974

    Article  CAS  Google Scholar 

  • Song YH, Wang XD, Rose RJ (2017) Oil body biogenesis and biotechnology in legume seeds. Plant Cell Rep 36:1519–1532

    Article  CAS  Google Scholar 

  • Thelen JJ, Ohlrogge JB (2002) Both antisense and sense expression of biotin carboxyl carrier protein isoform 2 inactivates the plastid acetyl-coenzyme A carboxylase in Arabidopsis thaliana. The Plant J 32:419–431

    Article  CAS  Google Scholar 

  • Ting JT, Lee K, Ratnayake C, Platt KA, Balsamo RA, Huang AH (1996) Oleosin genes in maize kernels having diverse oil contents are constitutively expressed independent of oil contents. Planta 199:158–165

    Article  CAS  Google Scholar 

  • Tzen JTC, Cao YZ, Laurent P, Ratnayake C, Huang AHC (1993) Lipids, proteins, and structure of seed oil bodies from diverse species. Plant Physiol 101:267–276

    Article  CAS  Google Scholar 

  • Wang FL, Zheng T, Wu GT, Lang CX, Hu ZH, Shi JH, Jin W, Chen JQ, Liu RH (2015) Overexpression of miR319a affects the balance between mitosis and endoreduplication in Arabidopsis leaves. Plant Mol Biol Rep 33:2006–2013

    Article  CAS  Google Scholar 

  • Warthmann N, Das S, Lanz C, Weigel D (2008) Comparative analysis of the MIR319a MicroRNA locus in Arabidopsis and related Brassicaceae. Mol Biol Evol 25:892–902

    Article  CAS  Google Scholar 

  • Wu YY, Chou YR, Wang CS, Tseng TH, Chen LJ, Tzen JTC (2010) Different effects on triacylglycerol packaging to oil bodies in transgenic rice seeds by specifically eliminating one of their two oleosin isoforms. Plant Physiol Bioch 48:81–89

    Article  CAS  Google Scholar 

  • Zhang D, Zhang HY, Hu ZB, Chu SS, Yu KY, Lv LL, Yang YM, Zhang XQ, Chen X, Kan GZ, Tang Y, Charles YQ, Yu DY (2019) Artificial selection on GmOLEO1 contributes to the increase in seed oil during soybean domestication. PLoS Genet 15(7):e1008267

    Article  Google Scholar 

Download references

Acknowledgments

We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (No. 31571700) and the Natural Science Foundation of Zhejiang Province (CN) (No. LY19C130005).

Author information

Authors and Affiliations

  1. Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, 298 Desheng Rd (M), Hangzhou, 310021, People’s Republic of China

    Fulin Wang, Tao Zheng, Zhanghua Hu, Guanting Wu, Chunxiu Lang & Renhu Liu

Authors
  1. Fulin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tao Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhanghua Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guanting Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunxiu Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renhu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renhu Liu.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Key Message

The overexpression of 35S:miR319a in transgenic Arabidopsis caused severely crinkled siliques and led to increased total oleosin levels. Electron microscopy revealed that the overexpression of miR319a in transgenic Arabidopsis seeds resulted in more numerous and smaller oil bodies. Changes in the size of oil bodies altered the lipid content and fatty acids component. Collectively, these results indicate that miR319a expression correlated with lipid metabolism.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, F., Zheng, T., Hu, Z. et al. Overexpression of miR319a Altered Oil Body Morphogenesis and Lipid Content in Arabidopsis Seeds. Plant Mol Biol Rep 38, 531–537 (2020). https://doi.org/10.1007/s11105-020-01217-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-020-01217-y

Keywords

Search

Navigation